Plant Molecular Biology

, Volume 16, Issue 6, pp 1009–1018 | Cite as

Comparison of the expression of several stress-responsive genes in potato tubers

  • Timothy M. Rickey
  • William R. Belknap


Changes in gene expression induced by mechanical injury and heat shock were studied by comparing the expression of several stress-responsive gene families in potato tubers. The steady-state levels of mRNA-encoding ubiquitin, HSP70, and phenylalanine ammonia-lyase (PAL) increased and patatin transcript levels decreased within 45 minutes of impact injury. Nuclear runoff assays were used to demonstrate that the changes in steady-state transcript levels were due, at least in part, to changes in the rate of transcription for these genes. The observed changes in transcript levels were confined to the injured portion of the tuber. Treatment of tubers with exogenous ethylene elicited the same changes in the steady-state transcript levels as impact injury, indicating a potential role for this hormone in the injury-induced regulation of these genes. Two other forms of physical stress, heat shock and cutting injury, resulted in patterns of gene expression that are different from those induced by impact injury. The stress-induced regulation of these four gene families is complex, even though several characteristics of their expression are similar.

Key words

heat shock HSP70 patatin phenylalanine ammonia-lyase ubiquitin wounding 


  1. 1.
    Altschuler M, Mascarenhas JP: Heat shock proteins and effects of heat shock in plants. Plant Mol Biol 1: 103–115 (1982).Google Scholar
  2. 2.
    Andrews D, Beames B, Summers MD, Park WD: Characterization of the lipid acyl hydrolase activity of the major potato (Solanum tuberosum) tuber protein, patatin, by cloning and abundant expression in a baculovirus vector. Biochem J 252: 199–206 (1988).PubMedGoogle Scholar
  3. 3.
    Belknap WR, Rickey TM, Rockhold DR: Blackspot bruise dependent changes in enzyme activity and gene expression in Lemhi Russet potato. Am Potato J 67: 253–265 (1990).Google Scholar
  4. 4.
    Bevan M, Shufflebottom D, Edwards K, Jefferson R, Schuch W: Tissue- and cell-specific activity of a phenylalanine ammonia-lyase promoter in transgenic plants. EMBO J 8: 1899–1906 (1989).PubMedGoogle Scholar
  5. 5.
    Chappell J, Hahlbrock K: Transcription of plant defence genes in response to UV light or fungal elicitor. Nature 311: 76–78 (1984).Google Scholar
  6. 6.
    Chen J, Varner JE: Isolation and characterization of cDNA clones for carrot extensin and a proline-rich 33-kDa protein. Proc Natl Acad Sci USA 82: 4399–4403 (1985).Google Scholar
  7. 7.
    Christensen AH, Quail PH: Sequence analysis and transcriptional regulation by heat shock of polyubiquitin transcripts from maize. Plant Mol Biol 12: 619–632 (1989).Google Scholar
  8. 8.
    Corbin DR, Sauer N, Lamb CJ: Differential regulation of a hydroxyproline-rich glycoprotein gene family in wounded and infected plants. Mol Cell Biol 7: 4337–4344 (1987).PubMedGoogle Scholar
  9. 9.
    Dalkin K, Bowles DJ: Local and systemic changes in gene expression induced in tomato plants by wounding and by elicitor treatment. Planta 179: 367–375 (1989).Google Scholar
  10. 10.
    Duck N, McCormick S, Winter J: Heat shock protein hsp70 cognate gene expression in vegetative and reproductive organs of Lycopersicon esculentum. Proc Natl Acad Sci USA 86: 3674–3678 (1989).Google Scholar
  11. 11.
    Ecker JR, Davis RW: Plant defense genes are regulated by ethylene. Proc Natl Acad Sci USA 84: 5202–5206 (1987).Google Scholar
  12. 12.
    Fritzemeier K-H, Cretin C, Kombrink E, Rohwer F, Taylor J, Scheel D, Hahlbrock K: Transient induction of phenylalanine ammonia-lyase and 4-coumarate: CoA ligase mRNAs in potato leaves infected with virulent or avirulent races of Phytophthora infestans. Plant Physiol 85: 34–41 (1987).Google Scholar
  13. 13.
    Craham JS, Hall G, Pearce G, Ryan CA: Regulation of synthesis of proteinase inhibitors I and II mRNAs in leaves of wounded plants. Planta 169: 399–405 (1986).Google Scholar
  14. 14.
    Hedrick SA, Bell JN, Boller T, Lamb CJ: Chitinase cDNA cloning and mRNA induction by fungal elicitor, Wounding, and infection. Plant Physiol 86: 182–186 (1988).Google Scholar
  15. 15.
    Heikkila JJ, Papp JET, Schultz GA, Bewley JD: Induction of heat shock protein messenger RNA in maize mesocotyls by water stress, abscisic acid, and wounding. Plant Physiol 76: 270–274 (1984).Google Scholar
  16. 16.
    Ho T-HD, Sachs MM: Stress-induced proteins: characterization and the regulation of their synthesis. In: Stumpf PK, Conn EE (eds) The Biochemistry of Plants: A Comprehensive Treatise, vol. 15, pp. 347–377. Academic Press, New York (1989).Google Scholar
  17. 17.
    Keller B, Schmid J, Lamb CJ: Vascular expression of a bean cell wall glycine-rich protein-β-glucuronidase gene fusion in transgenic tobacco. EMBO J 8: 1309–1314 (1989).Google Scholar
  18. 18.
    Kimpel JA, Key JL: Presence of heat shock mRNAs in field grown soybeans. Plant Physiol 79: 672–678 (1985).Google Scholar
  19. 19.
    Lawton MA, Lamb CJ: Transcriptional activation of plant defense genes by fungal elicitor, wounding, and infection. Mol Cell Biol 7: 335–341 (1987).PubMedGoogle Scholar
  20. 20.
    Liang X, Dron M, Cramer CL, Dixon RA, Lamb CJ: Differential regulation of phenylalanine ammonia-lyase genes during plant development and by environmental cues. J Biol Chem 264: 14486–14492 (1989).PubMedGoogle Scholar
  21. 21.
    Lindquist S: The heat shock response. Ann Rev Biochem 55: 1151–1191 (1986).CrossRefPubMedGoogle Scholar
  22. 22.
    Logemann J, Schell J, Willmitzer L: Improved method for the isolation of RNA from plant tissues. Anal Biochem 163: 16–20 (1987).PubMedGoogle Scholar
  23. 23.
    Logemann J, Mayer JE, Schell J, Willmitzer L: Differential expression of genes in potato tubers after wounding. Proc Natl Acad Sci USA 85: 1136–1140 (1988).Google Scholar
  24. 24.
    Luthe DS, Quatrano RS: Transcription in isolated wheat nuclei. II. Characterization of RNA synthesized in vitro. Plant Physiol 65: 309–313 (1980).Google Scholar
  25. 25.
    McKnight GS, Palmiter RD: Transcriptional regulation of the ovalbumin and conalbumin genes by steroid hormones in chick oviduct. J Biol Chem 254: 9050–9058 (1979).PubMedGoogle Scholar
  26. 26.
    Mignery GA, Pikaard CS, Hannapel DJ, Park WD: Isolation and sequence analysis of cDNA's for the major potato tuber storage protein, patatin. Nucl Acids Res 12: 7987–8000 (1984).PubMedGoogle Scholar
  27. 27.
    Monia BP, Ecker DJ, Crooke ST: New perspectives on the structure and function of ubiquitin. Bio/technology 8: 209–215 (1990).CrossRefGoogle Scholar
  28. 28.
    28. Murray MG, Thompson WF: Rapid isolation of high molecular weight plant DNA. Nuc Acids Res 8: 4321–4325.Google Scholar
  29. 29.
    Nairn CJ, Winesett L, Ferl RJ: Nucleotide sequence of an actin gene from Arabidopsis thaliana. Gene 65: 247–257 (1988).CrossRefPubMedGoogle Scholar
  30. 30.
    Pavek JJ, Corsini DL, Garner JG, Michener S, Sparks WC, Carnahan GF, Stranger CE, Mosley AR, Johnson MJ, Carter GE, Voss RE, Martin MW, Johansen RH: Lemhi Russet: A new high yielding variety with wide adaption, attractive tubers, and high internal quality. Am Potato J 58: 619–626 (1981).Google Scholar
  31. 31.
    Pena-Cortes H, Sanchez-Serrano J, Rocha-Sosa M, Willmitzer L: Systematic induction of proteinase-inhibitor-II gene expression in potato plants by wounding. Planta 174: 84–89 (1988).Google Scholar
  32. 32.
    Pena-Cortes H, Sanchez-Serrano JJ, Mertens R, Willmitzer L, Prat S: Abscisic acid is involved in the wound-induced expression of the proteinase inhibitor II gene in potato and tomato. Proc Natl Acad Sci USA 86: 9851–9855 (1989).Google Scholar
  33. 33.
    Racusen D: Lipid acyl hydrolase of patatin. Can J Bot 62: 1640–1644 (1984).Google Scholar
  34. 34.
    Rosahl S, Schell J, Willmitzer L: Expression of a tuber-specific storage protein in transgenic tobacco plants: demonstration of an esterase activity. EMBO J 6: 1155–1159 (1987).Google Scholar
  35. 35.
    Ryan CA: Oligosaccharide signalling in plants. Ann Rev Cell Biol 3: 295–317 (1987).PubMedGoogle Scholar
  36. 36.
    Ryder TB, Hedrick SA, Bell JN, Liang X, Clouse SD, Lamb CJ: Organization and differential activation of a gene family encoding the plant defense enzyme chalcone synthase in Phaseolus vulgaris. Mol Gen Genet 210: 219–233 (1987).PubMedGoogle Scholar
  37. 37.
    Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1989).Google Scholar
  38. 38.
    Sanchez-Serrano J, Schmidt R, Schell J, Willmitzer L: Nucleotide sequence of proteinase inhibitor II encoding cDNA of potato (Solanum tuberosum) and its mode of expression. Mol Gen Genet 203: 15–20 (1986).CrossRefGoogle Scholar
  39. 39.
    Stanford AL, Northcote DH, Bevan MW: Spatial and temporal patterns of transcription of a wound-induced gene in potato. EMBO J 9: 593–603 (1990).PubMedGoogle Scholar
  40. 40.
    Wingate VPM, Lawton MA, Lamb CJ: Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol 87: 206–210 (1988).Google Scholar
  41. 41.
    Winter J, Wright R, Duck N, Gasser C, Fraley R, Shah D: The inhibition of petunia hsp70 mRNA processing during CdCl2 stress. Mol Gen Genet 211: 315–319 (1988).CrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1991

Authors and Affiliations

  • Timothy M. Rickey
    • 1
  • William R. Belknap
    • 1
  1. 1.Western Regional Research Center, Agricultural Research ServiceUSDAAlbanyUSA

Personalised recommendations